The bacterial N-end rule pathway: Expect the unexpected

Molecular Microbiology

Volumn 76, Issue 3, 2010, Pages 545-558

  Dougan, D A ^a   Truscott, K N ^a   Zeth, K ^b  

^a LA TROBE UNIVERSITY   (Australia)

^b MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; ADENOSINE TRIPHOSPHATE; AMINO ACID DERIVATIVE; BACTERIAL ENZYME; BACTERIAL PROTEIN; PROTEIN CLPAP; PROTEIN CLPS; PROTEINASE; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; BACTERIAL METABOLISM; BACTERIAL STRAIN; CARBOXY TERMINAL SEQUENCE; ENZYME ACTIVITY; ENZYME SUBSTRATE; ESCHERICHIA COLI; EUKARYOTE; NONHUMAN; PRIORITY JOURNAL; PROKARYOTE; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN SYNTHESIS; SHORT SURVEY; BACTERIA; CHEMISTRY; GENETICS; METABOLISM; PROTEIN MOTIF;

BACTERIA (MICROORGANISMS); EUKARYOTA; PROKARYOTA;

AMINO ACID MOTIFS; BACTERIA; BACTERIAL PROTEINS; PROTEIN BIOSYNTHESIS; PROTEIN STABILITY;

EID: 77951567636     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2010.07120.x     Document Type: Short Survey

References (67)

1. Abramochkin, G. Shrader, T.E. (1996) Aminoacyl-tRNA recognition by the leucyl/phenylalanyl-tRNA-protein transferase. J Biol Chem 271 : 22901 22907. (Pubitemid 26304741)
2. Ades, S.E. (2008) Regulation by destruction: design of the sigmaE envelope stress response. Curr Opin Microbiol 11 : 535 540.
3. Andersson, F.I., Tryggvesson, A., Sharon, M., Diemand, A.V., Classen, M., Best, C., et al 2009) Structure and function of a novel type of ATP-dependent Clp protease. J Biol Chem 284 : 13519 13532.
4. Bachmair, A., Finley, D. Varshavsky, A. (1986) In vivo half-life of a protein is a function of its amino-terminal residue. Science 234 : 179 186. (Pubitemid 17186094)
5. Bachmair, A., Becker, F. Schell, J. (1993) Use of a reporter transgene to generate arabidopsis mutants in ubiquitin-dependent protein degradation. Proc Natl Acad Sci USA 90 : 418 421. (Pubitemid 23028873)
6. Baker, R.T. Varshavsky, A. (1991) Inhibition of the N-end rule pathway in living cells. Proc Natl Acad Sci USA 88 : 1090 1094. (Pubitemid 21916170)
7. Balzi, E., Choder, M., Chen, W.N., Varshavsky, A. Goffeau, A. (1990) Cloning and functional analysis of the arginyl-tRNA-protein transferase gene ATE1 of Saccharomyces cerevisiae. J Biol Chem 265 : 7464 7471. (Pubitemid 20162490)
8. Burns, K.E. Darwin, K.H. (2010) Pupylation versus ubiquitylation: tagging for proteasome-dependent degradation. Cell Microbiol 12 : 424 431.
9. Butler, S.M., Festa, R.A., Pearce, M.J. Darwin, K.H. (2006) Self-compartmentalized bacterial proteases and pathogenesis. Mol Microbiol 60 : 553 562.
10. Cranz-Mileva, S., Imkamp, F., Kolygo, K., Maglica, Z., Kress, W. Weber-Ban, E. (2008) The flexible attachment of the N-domains to the ClpA ring body allows their use on demand. J Mol Biol 378 : 412 424.
11. De Donatis, G.M., Singh, S.K., Viswanathan, S. Maurizi, M.R. (2010) A single ClpS monomer is sufficient to direct the activity of the ClpA hexamer. J Biol Chem 285 : 8771 8781.
12. Deutch, C.E. Soffer, R.L. (1975) Regulation of proline catabolism by leucyl,phenylalanyl-tRNA-protein transferase. Proc Natl Acad Sci USA 72 : 405 408.
13. Dougan, D.A., Mogk, A. Bukau, B. (2002a) Protein folding and degradation in bacteria: to degrade or not to degrade? That is the question. Cell Mol Life Sci 59 : 1607 1616. (Pubitemid 35346963)
14. Dougan, D.A., Reid, B.G., Horwich, A.L. Bukau, B. (2002b) ClpS, a substrate modulator of the ClpAP machine. Mol Cell 9 : 673 683. (Pubitemid 34273796)
15. Erbse, A., Schmidt, R., Bornemann, T., Schneider-Mergener, J., Mogk, A., Zahn, R., et al 2006) ClpS is an essential component of the N-end rule pathway in Escherichia coli. Nature 439 : 753 756. (Pubitemid 43237625)
16. Erbse, A.H., Wagner, J.N., Truscott, K.N., Spall, S.K., Kirstein, J., Zeth, K., et al 2008) Conserved residues in the N-domain of the AAA+ chaperone ClpA regulate substrate recognition and unfolding. FEBS J 275 : 1400 1410. (Pubitemid 351388792)
17. Flynn, J.M., Neher, S.B., Kim, Y.I., Sauer, R.T. Baker, T.A. (2003) Proteomic discovery of cellular substrates of the ClpXP protease reveals five classes of ClpX-recognition signals. Mol Cell 11 : 671 683.
18. Frottin, F., Martinez, A., Peynot, P., Mitra, S., Holz, R.C., Giglione, C. Meinnel, T. (2006) The proteomics of N-terminal methionine cleavage. Mol Cell Proteomics 5 : 2336 2349. (Pubitemid 46040638)
19. Gonda, D.K., Bachmair, A., Wunning, I., Tobias, J.W., Lane, W.S. Varshavsky, A. (1989) Universality and structure of the N-end rule. J Biol Chem 264 : 16700 16712.
20. Gottesman, S., Clark, W.P. Maurizi, M.R. (1990) The ATP-dependent Clp protease of Escherichia coli. Sequence of clpA and identification of a Clp-specific substrate. J Biol Chem 265 : 7886 7893. (Pubitemid 20158957)
21. Graciet, E., Hu, R.G., Piatkov, K., Rhee, J.H., Schwarz, E.M. Varshavsky, A. (2006) Aminoacyl-transferases and the N-end rule pathway of prokaryotic/eukaryotic specificity in a human pathogen. Proc Natl Acad Sci USA 103 : 3078 3083. (Pubitemid 43346427)
22. Graciet, E., Mesiti, F. Wellmer, F. (2009a) Structure and evolutionary conservation of the plant N-end rule pathway. Plant J 61 : 741 751.
23. Graciet, E., Walter, F., Maoileidigh, D.O., Pollmann, S., Meyerowitz, E.M., Varshavsky, A. Wellmer, F. (2009b) The N-end rule pathway controls multiple functions during Arabidopsis shoot and leaf development. Proc Natl Acad Sci USA 106 : 13618 13623.
24. Grigoryev, S., Stewart, A.E., Kwon, Y.T., Arfin, S.M., Bradshaw, R.A., Jenkins, N.A., et al 1996) A mouse amidase specific for N-terminal asparagine. The gene, the enzyme, and their function in the N-end rule pathway. J Biol Chem 271 : 28521 28532.
25. Guo, F., Esser, L., Singh, S.K., Maurizi, M.R. Xia, D. (2002) Crystal structure of the heterodimeric complex of the adaptor, ClpS, with the N-domain of the AAA+ chaperone, ClpA. J Biol Chem 277 : 46753 46762. (Pubitemid 35417678)
26. Hengge, R. (2009) Proteolysis of sigmaS (RpoS) and the general stress response in Escherichia coli. Res Microbiol 160 : 667 676.
27. Hinnerwisch, J., Fenton, W.A., Furtak, K.J., Farr, G.W. Horwich, A.L. (2005) Loops in the central channel of ClpA chaperone mediate protein binding, unfolding, and translocation. Cell 121 : 1029 1041. (Pubitemid 40894633)
28. Hou, J.Y., Sauer, R.T. Baker, T.A. (2008) Distinct structural elements of the adaptor ClpS are required for regulating degradation by ClpAP. Nat Struct Mol Biol 15 : 288 294.
29. Humbard, M.A., Miranda, H.V., Lim, J.M., Krause, D.J., Pritz, J.R., Zhou, G., et al 2010) Ubiquitin-like small archaeal modifier proteins (SAMPs) in Haloferax volcanii. Nature 463 : 54 60.
30. Hwang, C.S., Shemorry, A. Varshavsky, A. (2010) N-terminal acetylation of cellular proteins creates specific degradation signals. Science 327 : 973 977.
31. Jenal, U. (2009) The role of proteolysis in the Caulobacter crescentus cell cycle and development. Res Microbiol 160 : 687 695.
32. Kaji, A., Kaji, H. Novelli, G.D. (1965) Soluble amino acid-incorporating system. II. soluble nature of the system and the characterization of the radioactive product. J Biol Chem 240 : 1192 1197.
33. Kirstein, J., Schlothauer, T., Dougan, D.A., Lilie, H., Tischendorf, G., Mogk, A., et al 2006) Adaptor protein controlled oligomerization activates the AAA+ protein ClpC. EMBO J 25 : 1481 1491.
34. Kirstein, J., Dougan, D.A., Gerth, U., Hecker, M. Turgay, K. (2007) The tyrosine kinase McsB is a regulated adaptor protein for ClpCP. EMBO J 26 : 2061 2070. (Pubitemid 46625790)
35. Kress, W., Mutschler, H. Weber-Ban, E. (2009) Both ATPase domains of ClpA are critical for processing of stable protein structures. J Biol Chem 284 : 31441 31452.
36. Leibowitz, M.J. Soffer, R.L. (1969) A soluble enzyme from Escherichia coli which catalyzes the transfer of leucine and phenylalanine from tRNA to acceptor proteins. Biochem Biophys Res Commun 36 : 47 53.
37. Lo, J.H., Baker, T.A. Sauer, R.T. (2001) Characterization of the N-terminal repeat domain of Escherichia coli ClpA-A class I Clp/HSP100 ATPase. Protein Sci 10 : 551 559.
38. Lupas, A.N. Koretke, K.K. (2003) Bioinformatic analysis of ClpS, a protein module involved in prokaryotic and eukaryotic protein degradation. J Struct Biol 141 : 77 83.
39. Maglica, Z., Kolygo, K. Weber-Ban, E. (2009) Optimal efficiency of ClpAP and ClpXP chaperone-proteases is achieved by architectural symmetry. Structure 17 : 508 516.
40. Martin, A., Baker, T.A. Sauer, R.T. (2007) Distinct static and dynamic interactions control ATPase-peptidase communication in a AAA+ protease. Mol Cell 27 : 41 52. (Pubitemid 46991379)
41. Mayer, A., Siegel, N.R., Schwartz, A.L. Ciechanover, A. (1989) Degradation of proteins with acetylated amino termini by the ubiquitin system. Science 244 : 1480 1483. (Pubitemid 19171683)
42. Moliere, N. Turgay, K. (2009) Chaperone-protease systems in regulation and protein quality control in Bacillus subtilis. Res Microbiol 160 : 637 644.
43. Neuwald, A.F., Aravind, L., Spouge, J.L. Koonin, E.V. (1999) AAA+: a class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res 9 : 27 43. (Pubitemid 29095146)
44. Ninnis, R.L., Spall, S.K., Talbo, G.H., Truscott, K.N. Dougan, D.A. (2009) Modification of PATase by L/F-transferase generates a ClpS-dependent N-end rule substrate in Escherichia coli. EMBO J 28 : 1732 1744.
45. Rao, H., Uhlmann, F., Nasmyth, K. Varshavsky, A. (2001) Degradation of a cohesin subunit by the N-end rule pathway is essential for chromosome stability. Nature 410 : 955 959. (Pubitemid 32335844)
46. Roman-Hernandez, G., Grant, R.A., Sauer, R.T. Baker, T.A. (2009) Molecular basis of substrate selection by the N-end rule adaptor protein ClpS. Proc Natl Acad Sci USA 106 : 8888 8893.
47. Samsonova, N.N., Smirnov, S.V., Altman, I.B. Ptitsyn, L.R. (2003) Molecular cloning and characterization of Escherichia coli K12 ygjG gene. BMC Microbiol 3 : 2.
48. Scarpulla, R.C. Soffer, R.L. (1979) Regulation of proline dehydrogenase activity in Escherichia coli by leucyl-, phenylalanyl-tRNA:protein transferase. J Biol Chem 254 : 1724 1725.
49. Schmidt, R., Zahn, R., Bukau, B. Mogk, A. (2009) ClpS is the recognition component for Escherichia coli substrates of the N-end rule degradation pathway. Mol Microbiol 72 : 506 517.
50. Schrader, E.K., Harstad, K.G. Matouschek, A. (2009) Targeting proteins for degradation. Nat Chem Biol 5 : 815 822.
51. Schuenemann, V.J., Kralik, S.M., Albrecht, R., Spall, S.K., Truscott, K.N., Dougan, D.A. Zeth, K. (2009) Structural basis of N-end rule substrate recognition in Escherichia coli by the ClpAP adaptor protein ClpS. EMBO Rep 10 : 508 514.
52. Singh, S.K. Maurizi, M.R. (1994) Mutational analysis demonstrates different functional roles for the two ATP-binding sites in ClpAP protease from Escherichia coli. J Biol Chem 269 : 29537 29545.
53. Sprangers, R., Gribun, A., Hwang, P.M., Houry, W.A. Kay, L.E. (2005) Quantitative NMR spectroscopy of supramolecular complexes: dynamic side pores in ClpP are important for product release. Proc Natl Acad Sci USA 102 : 16678 16683. (Pubitemid 41688836)
54. Suto, K., Shimizu, Y., Watanabe, K., Ueda, T., Fukai, S., Nureki, O. Tomita, K. (2006) Crystal structures of leucyl/phenylalanyl-tRNA-protein transferase and its complex with an aminoacyl-tRNA analog. EMBO J 25 : 5942 5950. (Pubitemid 44967775)
55. Tasaki, T., Mulder, L.C., Iwamatsu, A., Lee, M.J., Davydov, I.V., Varshavsky, A., et al 2005) A family of mammalian E3 ubiquitin ligases that contain the UBR box motif and recognize N-degrons. Mol Cell Biol 25 : 7120 7136. (Pubitemid 41105909)
56. Tasaki, T., Zakrzewska, A., Dudgeon, D.D., Jiang, Y., Lazo, J.S. Kwon, Y.T. (2009) The substrate recognition domains of the N-end rule pathway. J Biol Chem 284 : 1884 1895.
57. Tobias, J.W., Shrader, T.E., Rocap, G. Varshavsky, A. (1991) The N-end rule in bacteria. Science 254 : 1374 1377. (Pubitemid 21917472)
58. Varshavsky, A. (1996) The N-end rule: functions, mysteries, uses. Proc Natl Acad Sci USA 93 : 12142 12149.
59. Vogtle, F.N., Wortelkamp, S., Zahedi, R.P., Becker, D., Leidhold, C., Gevaert, K., et al 2009) Global analysis of the mitochondrial N-proteome identifies a processing peptidase critical for protein stability. Cell 139 : 428 439.
60. Wang, J., Hartling, J.A. Flanagan, J.M. (1997) The structure of ClpP at 2.3 A resolution suggests a model for ATP-dependent proteolysis. Cell 91 : 447 456. (Pubitemid 27508234)
61. Wang, K.H., Roman-Hernandez, G., Grant, R.A., Sauer, R.T. Baker, T.A. (2008a) The molecular basis of N-end rule recognition. Mol Cell 32 : 406 414.
62. Wang, K.H., Oakes, E.S., Sauer, R.T. Baker, T.A. (2008b) Tuning the strength of a bacterial N-end rule degradation signal. J Biol Chem 283 : 24600 24607.
63. Wang, H., Piatkov, K.I., Brower, C.S. Varshavsky, A. (2009) Glutamine-specific N-terminal amidase, a component of the N-end rule pathway. Mol Cell 34 : 686 695.
64. Watanabe, K., Toh, Y., Suto, K., Shimizu, Y., Oka, N., Wada, T. Tomita, K. (2007) Protein-based peptide-bond formation by aminoacyl-tRNA protein transferase. Nature 449 : 867 871. (Pubitemid 47598606)
65. Weichart, D., Querfurth, N., Dreger, M. Hengge-Aronis, R. (2003) Global role for ClpP-containing proteases in stationary-phase adaptation of Escherichia coli. J Bacteriol 185 : 115 125. (Pubitemid 36008828)
66. Yu, A.Y. Houry, W.A. (2007) ClpP: a distinctive family of cylindrical energy-dependent serine proteases. FEBS Lett 581 : 3749 3757.
67. Zeth, K., Ravelli, R.B., Paal, K., Cusack, S., Bukau, B. Dougan, D.A. (2002) Structural analysis of the adaptor protein ClpS in complex with the N-terminal domain of ClpA. Nat Struct Biol 9 : 906 911. (Pubitemid 35417058)